Nocturnal swallowing augments arousal intensity and arousal tachycardia
Cortical arousal from sleep is associated with autonomic activation and acute increases in heart rate. Arousals vary considerably in their frequency, intensity/duration, and physiological effects. Sleep and arousability impact health acutely (daytime cognitive function) and long-term (cardiovascular...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2020-04, Vol.117 (15), p.8624-8632 |
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creator | Burke, P. G. R. Carter, S. G. Knapman, F. Patti, J. Butlin, M. Gandevia, S. C. Butler, J. E. Eckert, D. J. Bilston, L. E. |
description | Cortical arousal from sleep is associated with autonomic activation and acute increases in heart rate. Arousals vary considerably in their frequency, intensity/duration, and physiological effects. Sleep and arousability impact health acutely (daytime cognitive function) and long-term (cardiovascular outcomes). Yet factors that modify the arousal intensity and autonomic activity remain enigmatic. In this study of healthy human adults, we examined whether reflex airway defense mechanisms, specifically swallowing or glottic adduction, influenced cardiac autonomic activity and cortical arousal from sleep. We found, in all subjects, that swallows trigger rapid, robust, and patterned tachycardia conserved across wake, sleep, and arousal states. Tachycardia onset was temporally matched to glottic adduction—the first phase of swallow motor program. Multiple swallows increase the magnitude of tachycardia via temporal summation, and blood pressure increases as a function of the degree of tachycardia. During sleep, swallows were overwhelmingly associated with arousal. Critically, swallows were causally linked to the intense, prolonged cortical arousals and marked tachycardia. Arousal duration and tachycardia increased in parallel as a function of swallow incidence. Our findings suggest that cortical feedback and tachycardia are integrated responses of the swallowmotor program. Our work highlights the functional influence of episodic, involuntary airway defense reflexes on sleep and vigilance and cardiovascular function in healthy individuals. |
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G. R. ; Carter, S. G. ; Knapman, F. ; Patti, J. ; Butlin, M. ; Gandevia, S. C. ; Butler, J. E. ; Eckert, D. J. ; Bilston, L. E.</creator><creatorcontrib>Burke, P. G. R. ; Carter, S. G. ; Knapman, F. ; Patti, J. ; Butlin, M. ; Gandevia, S. C. ; Butler, J. E. ; Eckert, D. J. ; Bilston, L. E.</creatorcontrib><description>Cortical arousal from sleep is associated with autonomic activation and acute increases in heart rate. Arousals vary considerably in their frequency, intensity/duration, and physiological effects. Sleep and arousability impact health acutely (daytime cognitive function) and long-term (cardiovascular outcomes). Yet factors that modify the arousal intensity and autonomic activity remain enigmatic. In this study of healthy human adults, we examined whether reflex airway defense mechanisms, specifically swallowing or glottic adduction, influenced cardiac autonomic activity and cortical arousal from sleep. We found, in all subjects, that swallows trigger rapid, robust, and patterned tachycardia conserved across wake, sleep, and arousal states. Tachycardia onset was temporally matched to glottic adduction—the first phase of swallow motor program. Multiple swallows increase the magnitude of tachycardia via temporal summation, and blood pressure increases as a function of the degree of tachycardia. During sleep, swallows were overwhelmingly associated with arousal. Critically, swallows were causally linked to the intense, prolonged cortical arousals and marked tachycardia. Arousal duration and tachycardia increased in parallel as a function of swallow incidence. Our findings suggest that cortical feedback and tachycardia are integrated responses of the swallowmotor program. Our work highlights the functional influence of episodic, involuntary airway defense reflexes on sleep and vigilance and cardiovascular function in healthy individuals.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1907393117</identifier><identifier>PMID: 32229567</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Arousal ; Biological Sciences ; Blood pressure ; Cardiac arrhythmia ; Cardiovascular system ; Cerebral cortex ; Cognitive ability ; Defense programs ; Heart rate ; Physiological effects ; PNAS Plus ; Reflexes ; Respiratory tract ; Sleep ; Sleep and wakefulness ; Swallowing ; Tachycardia ; Vigilance</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2020-04, Vol.117 (15), p.8624-8632</ispartof><rights>Copyright National Academy of Sciences Apr 14, 2020</rights><rights>2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-e964f6bc450f0950dde4dc2a901f87ba8aadce1dbc1d78cc63942c3b7667e7523</citedby><cites>FETCH-LOGICAL-c443t-e964f6bc450f0950dde4dc2a901f87ba8aadce1dbc1d78cc63942c3b7667e7523</cites><orcidid>0000-0003-3503-2363 ; 0000-0003-0829-5934 ; 0000-0002-5784-9043 ; 0000-0002-6896-3298</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26930919$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26930919$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27923,27924,53790,53792,58016,58249</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32229567$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Burke, P. G. R.</creatorcontrib><creatorcontrib>Carter, S. G.</creatorcontrib><creatorcontrib>Knapman, F.</creatorcontrib><creatorcontrib>Patti, J.</creatorcontrib><creatorcontrib>Butlin, M.</creatorcontrib><creatorcontrib>Gandevia, S. C.</creatorcontrib><creatorcontrib>Butler, J. E.</creatorcontrib><creatorcontrib>Eckert, D. J.</creatorcontrib><creatorcontrib>Bilston, L. E.</creatorcontrib><title>Nocturnal swallowing augments arousal intensity and arousal tachycardia</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Cortical arousal from sleep is associated with autonomic activation and acute increases in heart rate. Arousals vary considerably in their frequency, intensity/duration, and physiological effects. Sleep and arousability impact health acutely (daytime cognitive function) and long-term (cardiovascular outcomes). Yet factors that modify the arousal intensity and autonomic activity remain enigmatic. In this study of healthy human adults, we examined whether reflex airway defense mechanisms, specifically swallowing or glottic adduction, influenced cardiac autonomic activity and cortical arousal from sleep. We found, in all subjects, that swallows trigger rapid, robust, and patterned tachycardia conserved across wake, sleep, and arousal states. Tachycardia onset was temporally matched to glottic adduction—the first phase of swallow motor program. Multiple swallows increase the magnitude of tachycardia via temporal summation, and blood pressure increases as a function of the degree of tachycardia. During sleep, swallows were overwhelmingly associated with arousal. Critically, swallows were causally linked to the intense, prolonged cortical arousals and marked tachycardia. Arousal duration and tachycardia increased in parallel as a function of swallow incidence. Our findings suggest that cortical feedback and tachycardia are integrated responses of the swallowmotor program. Our work highlights the functional influence of episodic, involuntary airway defense reflexes on sleep and vigilance and cardiovascular function in healthy individuals.</description><subject>Arousal</subject><subject>Biological Sciences</subject><subject>Blood pressure</subject><subject>Cardiac arrhythmia</subject><subject>Cardiovascular system</subject><subject>Cerebral cortex</subject><subject>Cognitive ability</subject><subject>Defense programs</subject><subject>Heart rate</subject><subject>Physiological effects</subject><subject>PNAS Plus</subject><subject>Reflexes</subject><subject>Respiratory tract</subject><subject>Sleep</subject><subject>Sleep and wakefulness</subject><subject>Swallowing</subject><subject>Tachycardia</subject><subject>Vigilance</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNpdkUtP4zAUhS3ECAoza1agSmzYBPyKHW-QUMVLQjMbWFs3jlNSpXaxHVD_Pc4UCjMrWz6fz30chI4IPidYsouVg3hOVL4qRojcQROCFSkEV3gXTTCmsqg45fvoIMYFxliVFd5D-4xSqkohJ-j2tzdpCA76aXyDvvdvnZtPYZgvrUtxCsEPMWudS9bFLq2n4JrtawLzvDYQmg5-oh8t9NH--jgP0dPN9ePsrnj4c3s_u3ooDOcsFVYJ3ora8BK3uRncNJY3hoLCpK1kDRVAYyxpakMaWRkjmOLUsFoKIa0sKTtElxvf1VAvbWZdCtDrVeiWENbaQ6f_VVz3rOf-VUsiSl6V2eDswyD4l8HGpJddNLbvwdk8laasKqmkXIy1Tv9DF_7vqkZq3DeulMzUxYYywccYbLtthmA9hqTHkPRXSPnHyfcZtvxnKhk43gCLmHzY6lQoltNV7B2eC5mQ</recordid><startdate>20200414</startdate><enddate>20200414</enddate><creator>Burke, P. 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G. R.</au><au>Carter, S. G.</au><au>Knapman, F.</au><au>Patti, J.</au><au>Butlin, M.</au><au>Gandevia, S. C.</au><au>Butler, J. E.</au><au>Eckert, D. J.</au><au>Bilston, L. E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nocturnal swallowing augments arousal intensity and arousal tachycardia</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2020-04-14</date><risdate>2020</risdate><volume>117</volume><issue>15</issue><spage>8624</spage><epage>8632</epage><pages>8624-8632</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Cortical arousal from sleep is associated with autonomic activation and acute increases in heart rate. Arousals vary considerably in their frequency, intensity/duration, and physiological effects. Sleep and arousability impact health acutely (daytime cognitive function) and long-term (cardiovascular outcomes). Yet factors that modify the arousal intensity and autonomic activity remain enigmatic. In this study of healthy human adults, we examined whether reflex airway defense mechanisms, specifically swallowing or glottic adduction, influenced cardiac autonomic activity and cortical arousal from sleep. We found, in all subjects, that swallows trigger rapid, robust, and patterned tachycardia conserved across wake, sleep, and arousal states. Tachycardia onset was temporally matched to glottic adduction—the first phase of swallow motor program. Multiple swallows increase the magnitude of tachycardia via temporal summation, and blood pressure increases as a function of the degree of tachycardia. During sleep, swallows were overwhelmingly associated with arousal. Critically, swallows were causally linked to the intense, prolonged cortical arousals and marked tachycardia. Arousal duration and tachycardia increased in parallel as a function of swallow incidence. 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subjects | Arousal Biological Sciences Blood pressure Cardiac arrhythmia Cardiovascular system Cerebral cortex Cognitive ability Defense programs Heart rate Physiological effects PNAS Plus Reflexes Respiratory tract Sleep Sleep and wakefulness Swallowing Tachycardia Vigilance |
title | Nocturnal swallowing augments arousal intensity and arousal tachycardia |
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